Performance of Immatures of Three Neotropical Miridae at Five Different Temperatures, Reared on Ephestia Kuehniella Eggs on Tobacco Plants
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Bulletin of Insectology 71 (1): 77-87, 2018 ISSN 1721-8861 Performance of immatures of three Neotropical Miridae at five different temperatures, reared on Ephestia kuehniella eggs on tobacco plants 1 1 2 1 Vanda Helena Paes BUENO , Flavio Cardoso MONTES , Marcus Vinicius SAMPAIO , Ana Maria CALIXTO , 3 Joop C. VAN LENTEREN 1Laboratory of Biological Control, Department of Entomology, Federal University of Lavras, MG, Brazil 2Institute of Agricultural Sciences, Federal University of Uberlândia, MG, Brazil 3Laboratory of Entomology, Wageningen University, The Netherlands Abstract Effects of temperature (16, 20, 24, 28 and 32 ± 1 °C), host plant (Nicotiana tabacum L.) and factitious prey (eggs of Ephestia kuehniella Zeller) on immature development of three recently found Neotropical mirids, Campyloneuropsis infumatus (Carvalho), Engytatus varians (Distant) and Macrolophus basicornis (Stal) were studied at RH 70 ± 10% and 12h photophase in climate cabi- nets. These mirids are being evaluated for biological control of the South American tomato borer Tuta absoluta (Meyrick) and other pests on tomato. Survival of eggs of the three mirid species on tobacco was high (> 80%) at 16-28 °C, but lower (< 80%) at 32 °C. Development times decreased with increasing temperature from 16-28 °C. Nymphal survival was higher (84-96%) at 20, 24 and 28 °C than at 16 and 32 °C (46-83%). The sex ratio of C. infumatus was strongly female biased at all temperatures, whereas it was 1:1 for the other two species. The lower temperature thresholds for egg-adult development of C. infumatus, E. varians and M. basicornis were 9.4, 9.4 and 7.9 °C, and their thermal constants were 384.6, 384.6 and 476.2 DD, respectively. Temperatures between 24 to 28 °C are best for immature performance and for rearing of these mirids species. Eggs of the facti- tious host E. kuehniella provide adequate food for their mass production. Optimal temperatures for best mirid predator perform- ance are similar to those for the pest T. absoluta, indicating good climate matching. Key words: Campyloneuropsis infumatus, Engytatus varians, Macrolophus basicornis, Tuta absoluta, biological control, mass production, thermal constants. Introduction coris tenuis (Reuter) (Hemiptera Miridae) are effec- tively controlling T. absoluta and Bemisia tabaci (Gen- Tomato Solanum lycopersicum L. (Solanaceae) is the nadius) (Calvo et al., 2012). In Brazil, the species Cam- most widely produced fruit vegetable in the world and pyloneuropsis infumatus (Carvalho), Engytatus varians also plays an important role in the agricultural economy (Distant) and Macrolophus basicornis (Stal) (Hemiptera of Brazil, one of the main tomato producers worldwide Miridae) were recently found in the laboratory and field (Agrianual, 2016). Tomato can be attacked by various to prey on eggs and larvae of T. absoluta (Bueno et al., insect pests, including the South American tomato borer 2013a; 2013b; van Lenteren et al., 2017), nymphs of Tuta absoluta (Meyrick) (Lepidoptera Gelechiidae), B. tabaci and eggs and larvae of various other lepidop- which may cause complete crop loss without pest con- teran pests of tomato (Bueno et al. 2013a). Bueno et al. trol (Guedes and Picanço, 2012). In Brazil, T. absoluta (2012; 2013a; 2013b) and Silva et al. (2016) reported is controlled by frequent pesticide sprays (Thomazini et that these Neotropical mirids can use tomato plants as al., 2001) and as a consequence, Brazilian tomato borer an oviposition substrate, can complete their develop- populations have acquired resistance to several active ment on it, and, contrary to other predators, like Geoco- ingredients, resulting in a so-named pesticide treadmill, ris punctipes (Say) (Hemiptera Geocoridae) and Orius decimation of natural enemies and high residue levels insidiosus (Say) (Hemiptera Anthocoridae), can easily on the tomato fruit (van den Bosch, 1978; Siqueira et walk on the stems of tomato plants despite the presence al., 2000; 2001; Silva et al., 2011; Guedes and Picanço, of sticky and poisonous trichomes (Bueno et al., 2013a). 2012). The rapid development of resistance to fre- Predatory Miridae show the characteristic of zoophyto- quently applied pesticides necessitates a search for al- phagy: in addition to eat animal prey, they also feed on ternative control methods, such as biological control. plant tissues to complement or supplement nutritional Heteropteran predators, particularly those belonging to needs or as a source of water (Wheeler, 2001; Albajes the family Miridae (Calvo et al., 2012; van Lenteren, and Alomar, 2008; Bueno and van Lenteren, 2012). 2012; Jaworski et al., 2013; Pazyuk et al., 2014; van Phytophagy can result in both beneficial and detrimental Lenteren et al., 2018a) might provide control of T. abso- effects. Beneficial because plant feeding allows them to luta, while these polyphagous predators may also be survive periods of low pest abundance, detrimental be- used for control of other key pests of tomato (Calvo et cause it may result in plant injury and yield loss. The al., 2009; Martínez et al., 2015; Pérez-Hedo et al, two mirids commercially used for biological control of 2015). In Spain, for example, the Palearctic mirid Mac- important pests in greenhouse tomatoes, M. pygmaeus rolophus pygmaeus (Rambur) and Paleaotropic Nesidio- and N. tenuis, may cause serious plant injury under spe- cific conditions when prey availability is low and preda- for egg-adult development, and sex ratio of emerged tor density is high. Particularly N. tenuis needs special adults of C. infumatus, E. varians and M. basicornis at attention with regard to population management at high five temperatures (16, 20, 24, 28 and 32 ± 1 °C) with densities in combination with low pest populations, be- E. kuehniella eggs as food source and with tobacco as cause extensive plant feeding by this predator results in host plant. This temperature range was selected based necrotic rings on the stems, shoots, leaf petioles and on the optimum temperatures for tomato production in flower stalks, causing abortion of flowers and young Brazil (Naika et al., 2006), though lower and higher fruits, reduced growth of tomato plants and yield loss temperatures may occasionally occur. Both, growers (Calvo et al., 2009). However, when properly managed, producing tomatoes in the field and in greenhouses try the European mirids are considered important biocontrol to adhere at these optimal temperature schedules. agents in tomato IPM and are used on a large scale in the Meditarranean region (Pérez-Hedo and Urbaneja, 2016). Remarkably, nymphs and adults of the three Materials and methods zoophytophagous Neotropical mirids appeared to cause little injury to tomato seedlings and fruit, even when Rearing of the mirid predators present in high densities and in the absence of prey in Adult mirids (C. infumatus, E. varians and M. basi- the laboratory (Silva et al., 2017a) and in presence of cornis) were collected in areas cultivated with tomato prey in the greenhouse (van Lenteren et al., 2018b). (S. lycopersicum) and tobacco Nicotiana tabacum L. However, the potential of these Neotropical mirids to (Solanaceae) (Bueno et al., 2012). Subsequently, a rear- control pest populations of T. absoluta in the field still ing colony was set up in the laboratory as described in remains to be demonstrated. Knowledge about the Bueno et al. (2013a). Tobacco plants, N. tabacum cv predator’s activity at a range of temperatures occurring TNN were grown in a greenhouse on organic substrate in the field and in greenhouses in tomato production ar- (75% Pinus rusk and 25% vermiculite). Seedlings with eas of Brazil is important to be able to determine their two pairs of leaves were transplanted to 2 L plastic pots potential as natural enemies for control of T. absoluta and maintained until attaining a height of 25 cm. Field and other pests on tomato. Also, information about their collected adults of each predator species were individu- lower temperature threshold and thermal constant assists ally released in acrylic cages (60 × 30 × 30 cm) contain- in determining their periods of activity in the field. ing a tobacco plant as oviposition substrate and a water Hughes et al. (2010) reported that a predator would source. Tobacco plants and the adult predators remained have a selective advantage over its prey if it has a lower in the cages for seven days. Then, the plants containing temperature threshold and a smaller thermal constant mirid eggs were transferred to new cages. Eggs of than its prey, because it would have a greater number of E. kuehniella were offered ad libitum as food to the mirid generations per year and would be active over a wider nymphs and adults twice weekly. The stock rearings range of temperatures than the prey. On the other hand, were kept in a climate room at 25 ± 1 °C, RH 70 ± 10% synchronization of the life history of the predator to that and 12 h photophase. of its prey is important at a range of local tomato pro- duction climate conditions (van Lenteren, 2010; Clarke, Development, survival and morphological aspects 2017). Interestingly, Horn (1998) found that biological of eggs control agents often have optimal development tempera- Ten pairs of each predator species were released in tures that are different from their prey. glass pots (1.7 L) containing a plastic cup (200 mL) Mass rearing of natural enemies is a critical step in a (8.5 cm diameter × 5.5 cm height) with a tobacco seed- biological control programme. Thus, information about ling with two pairs of leaves as oviposition substrate responses to different temperatures and thermal re- and E. kuehniella eggs as food ad libitum for a 24h pe- quirements of these Brazilian mirid predators can also riod. The glass pots were sealed with voile fabric and assist in designing an efficient mass rearing system and kept in a climate room at 25 ± 1 °C, RH 70 ± 10% and in estimating the success of establishment after release 12 h photophase.